Single-neuron responses to intraoral delivery of odor solutions in primary olfactory and gustatory cortex

Abstract

Smell plays a major role in our perception of food. Odorants released inside the mouth during consumption are combined with taste and texture qualities of a food to guide flavor preference learning and food choice behavior. Here, we built on recent physiological findings that implicated primary sensory cortex in multisensory flavor processing. Specifically, we used extracellular recordings in awake rats to characterize responses of single neurons in primary olfactory (OC) and gustatory cortex (GC) to intraoral delivery of odor solutions and compare odor responses to taste and plain water responses. The data reveal responses to olfactory, oral somatosensory, and gustatory qualities of intraoral stimuli in both OC and GC. Moreover, modality-specific responses overlap in time, indicating temporal convergence of multisensory, flavor-related inputs. The results extend previous work suggesting a role for primary OC in mediating influences of taste on smell that characterize flavor perception and point to an integral role for GC in olfactory processing.NEW & NOTEWORTHY Food perception is inherently multisensory, taking into account taste, smell, and texture qualities. However, the neural mechanisms underlying flavor perception remain unknown. Recording neural activity directly from the rat brain while animals consume multisensory flavor stimuli, we demonstrate that information about odor, taste, and mouthfeel of food converges on primary taste and smell cortex. The results suggest that processing of naturalistic, multisensory information involves an interacting network of primary sensory areas.

Keywords: electrophysiology; flavor; gustatory cortex; multisensory; olfactory cortex.

Fig. 1.

Electrode implant location. DAPI-stained (blue) coronal brain sections showing the reconstructed location of electrodes implanted in olfactory (piriform) cortex (bregma = −1.4 mm; A) and gustatory (insular) cortex (bregma = +1.6 mm; B), indicated by DiI labeling (pink).

Fig. 2.

Stimulus presentation protocols. A: during passive presentation, drops of fluid are delivered into the oral cavity via intraoral cannulas (IOC) at random intertrial intervals (ITI). B: during active acquisition, illuminating LEDs in a nose poke signals the availability of a stimulus (cue light). Stimulus delivery occurs upon the animal breaking an infrared beam in the nose poke, and consists of simultaneous presentation of 1) an orthonasal stimulus; and 2) a drop of fluid into the oral cavity via IOC. A water reward (delivered via IOC) is presented when the animal holds its nose in the nose poke for the duration of the orthonasal stimulus. After completion of a trial, the nose poke is unresponsive for a random ITI, indicated by turning off the cue light. Two trials are shown for each protocol, separated by dashes lines.

Fig. 3.

Single olfactory (OC) and gustatory cortex (GC) neuron responses to intraoral delivery of odor solutions. Example single trial raster diagrams (i and ii) and responses profiles (iii and iv) of single OC (blue) and GC (red) neuron responses to odor solutions (colored lines) and plain water (gray lines) relative to stimulus delivery. Profiles are averaged (±SE) over trials (n = 10 per condition). Insets: randomly selected action potential waveforms (n = 100) for each neuron.

Fig. 4.

Population responses to intraoral delivery of odor solutions. A and B: absolute magnitude of the response to odor solutions (colored lines) and plain water (black lines), averaged (±SE) over all stimulus-responsive neuron-odor pairs in OC (blue, n = 74; A) and GC (red, n = 66; B). C: occurrence of significant odor-specific responses for individual neuron-odor pairs in OC and GC. D: proportion (out of all stimulus responsive neuron-odor pairs) of neuron-odor pairs exhibiting significant odor-specific modulations over time in OC and GC. E: absolute magnitude of the difference in response to water and odor solution, averaged (±SE) over all responses that exhibited significant odor-specific modulations in OC (n = 11) and GC (n = 12).

Fig. 5.

Intraoral odor-selectivity of single OC and GC neurons. A and B: firing rate (A) and z-normalized response magnitude (B) during the stimulus period (relative to water) for all pairs of intra-orally delivered odorants recorded from the same neurons in OC (dark gray, n = 49) and GC (light gray, n = 33). Each circle represents a pair of responses: filled circles indicate pairs for which both responses showed a significant odor-specific response period; dotted circles indicate pairs for which only one of the responses showed a significant odor-specific response period; open circles indicate pairs for which none of the responses showed a significant odor-specific period. Diagonal line indicates identical responses to both odors.

Fig. 6.

OC responses to intraoral odor solutions are modulated by respiration. A: examples of respiration and spiking activity of a single OC neuron recorded during 2 trials during which odor solution was delivered intraorally. B: frequency spectra of respiration and spiking activity during the stimulus period, averaged over trials for all recording sessions (n = 3) and stimulus-responsive neuron-odor pairs (n = 24), respectively. C: coherence as a function of frequency and time relative to intraoral delivery of odor solutions, averaged over all stimulus-responsive neuron-odor pairs. D: coherence between respiration and spiking activity during 1.5 s following intraoral delivery of odor solutions, averaged (±SE) over all stimulus-responsive neuron-odor pairs.

Fig. 7.

Population response of OC and GC neurons to taste solutions. A: occurrence of significant taste-specific responses for individual neuron-taste pairs in OC (blue) and GC (red). B: proportion of neuron-taste pairs (out of all stimulus responsive neuron-taste pairs, n = 23 and 33 in OC and GC, respectively) exhibiting significant taste-specific modulations over time in OC and GC. C: absolute magnitude of the difference in response to water and taste solution, averaged (±SE) over all responses that exhibited significant taste-specific modulations in OC (n = 5) and GC (n = 13).

Fig. 8.

Comparison of intraoral and orthonasal odor presentation mode. A: examples of single OC (i and ii) and GC (iii and iv) neuron responses to the same odorants presented intraorally (dark gray) and orthonasally (light gray) relative to stimulus delivery, averaged (±SE) over trials (n = 5-10 per condition). Insets: randomly selected action potential waveforms (n = 100) for each neuron. B and C: firing rate (B) and z-normalized response magnitude (C) during the stimulus period relative to control, in intraoral vs. orthonasal modes, for all stimulus-responsive neuron-odor pairs in OC (dark gray, n = 26) and GC (light gray, n = 32).